Acclimation to different depths by the marine angiosperm Posidonia oceanica: transcriptomic and proteomic profiles
SUPPLEMENTARY MATERIAL
The Supplementary Material for this article can be found online at: http://www.frontiersin.org/PlantProteomics/10.3389/
fpls.2013.00195/abstract
Figure S1 | RT-qPCR SSH library.Expression levels of Pooc_B_c42 and Pooc_B_c 217 (y-axis, Mean± SD) in Posidonia oceanica shoots collected at−25 m (deep-library). Shoots collected at −5 m (shallo-library) were used as control and the expression level of GOI in the control is represented in the figure by the x-axis. RT-qPCR data were normalized (A) with the best RGs in this experimental condition (EF1A, L23, NTUBC, Serra et al., 2012b), (B) using “universal” RGs (EF1A, NTUBC, 18S, and UBI) (*p< 0.05, ***p < 0.001). Additional information on primers sequences and RT-qPCR conditions inSerra et al. (2012b).
Table S1 | Additional statistics features of SSH–EST library.Additional statistics features of SSH–ESTs Posidonia oceanica library.
Table S2a | List of Unigenes belonging to the shallow (high-light) library.
List of Unigenes belonging to the shallow (high-light) library. Unigenes name, their functional annotation with the E-value, number of ESTs identified (S_EST) and sequences lengths (Length) are indicated. For each sequence, the presence of putative ORF (open reading frame), SSRs (simple sequences repeats) and SNPs (single-nucleotide polymorphisms) are also showed.
Table S2b | List of Unigenes belonging to the deep (low-light) library.List of Unigenes belonging to the deep (low-light) library. Unigenes name, their functional annotation with the E-value, number of ESTs identified (S_EST) and sequences lengths (Length) are indicated. For each sequence, the presence of putative ORF (open reading frame), SSRs (simple sequences repeats) and SNPs (single-nucleotide polymorphisms) are also showed.
Table S3a | List of peptides identified in the 1DE gel of proteins from shallow samples (S).List of peptides identified in the slices of 1DE gel of proteins from shallow samples (S), the protein attribution obtained with GPM and X!TANDEM sotfwares with the corresponding log(e) value, functional annotation obtained with TBLASTN search against Dr.Zompo database and corresponding E-value are shown.
Table S3b | List of peptides identified 1DE gel of proteins from deep samples (D).List of peptides identified in the slices of 1DE gel of proteins from deep samples (D), the protein attribution obtained with GPM and X!TANDEM softwares with the corresponding log(e) value, functional annotation obtained with TBLASTN search against Dr.Zompo database and corresponding E-value are shown.
REFERENCES
Alba, R., Fei, Z., Payton, P., Liu, Y., Moore, S. L., Debbie, P., et al. (2004). ESTs, cDNA microarrays, and gene expres-sion profiling: tools for dissecting plant physiology and develop-ment. Plant J. 39, 697–714. doi:
10.1111/j.1365-313X.2004.02178.x Ardizzone, G., Belluscio, A., and
Maiorano, L. (2006). Long-term change in the structure of a
Posidonia oceanica landscape and its reference for a monitoring plan. Mar. Ecol. 27, 299–309. doi:
10.1111/j.1439-0485.2006.00128.x Armengaud, J. (2009). A perfect
genome annotation is within reach with the proteomics and genomics alliance. Curr. Opin.
Microbiol. 12, 292–300. doi:
10.1016/j.mib.2009.03.005 Arnaud-Haond, S., Duarte, C. M.,
Diaz-Almela, E., Marbà, N.,
Sintes, T., and Serrão, E. A.
(2012). Implications of extreme life span in clonal organisms:
millenary clones in meadows of the threatened seagrass Posidonia oceanica. PLoS ONE 7:e30454. doi:
10.1371/journal.pone.0030454 Blokhina, O. (2003). Antioxidants,
oxidative damage and oxygen deprivation stress: a review. Ann.
Bot. 91, 179–194. doi: 10.1093/
aob/mcf118
Bruno, A., Bruno, L., Chiappetta, A., Giannino, D., and Bitonti, M. B.
(2010). PoCHL P expression pattern in Posidonia oceanica is related to critical light conditions. Mar. Ecol.
Prog. Ser. 415, 61–71.
Buia, M., and Mazzella, L. (1991).
Reproductive phenology of the Mediterranean seagrasses Posidonia oceanica (L.) Delile, Cymodocea nodosa (Ucria) Aschers., and Zostera noltii Hornem. Aquat. Bot.
Frontiers in Plant Science | Plant Proteomics June 2013 | Volume 4 | Article 195|12
Dattolo et al. Posidonia oceanica acclimation at depth
40, 343–362. doi: 10.1016/0304-3770(91)90080-O
Bunney, T. D., Van Walraven, H. S., and De Boer, aH. (2001). 14-3-3 protein is a regulator of the mito-chondrial and chloroplast ATP syn-thase. Proc. Natl. Acad. Sci. U.S.A.
98, 4249–4254. doi: 10.1073/pnas.
061437498
Casazza, G., and Mazzella, L. (2002).
Photosynthetic pigment composi-tion of marine angiosperms: prelim-inary characterization of mediter-ranean seagrasses. Gianna Casazza and Lucia Mazzella. Bull. Sci. Mar.
71, 1171–1181.
Chang, S., Puryear, J., and Cairney, J. (1993). A simple and efficient method for isolating RNA from pine trees. Plant Mol. Biol. Rep. 11, 113–116. doi: 10.1007/BF02670468 Chevalier, F., Martin, O., Rofidal,
V., Devauchelle, A.-D., Barteau, S., Sommerer, N., et al. (2004).
Proteomic investigation of natural variation between Arabidopsis ecotypes. Proteomics 4, 1372–1381.
doi: 10.1002/pmic.200300750 Chitnis, P. R. (2001). PHOTOSYSTEM
I: function and physiology.
Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 593–626. doi:
10.1146/annurev.arplant.52.1.593 Cobbett, C. S. (2000). Update on heavy
metal stress phytochelatins and their roles in heavy metal detoxification.
Plant Physiol. 123, 825–832. doi:
10.1104/pp.123.3.825
Costanza, R. (1997). The value of world’ecosystem services and nat-ural capital. Nature 287, 253–260.
doi: 10.1038/387253a0
Cozza, R., Pangaro, T., Maestrini, P., Giordani, T., Natali, L., and Cavallini, A. (2006). Isolation of putative type 2 metalloth-ionein encoding sequences and spatial expression pattern in the seagrass Posidonia oceanica.
Aquat. Bot. 85, 317–323. doi:
10.1016/j.aquabot.2006.06.010 Craig, R., and Beavis, R. C. (2003).
A method for reducing the time required to match protein sequences with tandem mass spectra. Rapid Commun. Mass Spectrom. 17, 2310–2316. doi: 10.1002/rcm.1198 Craig, R., Cortens, J. P., and Beavis,
R. C. (2004). Open source system for analyzing, validating, and stor-ing protein identification data. J.
Proteome Res. 3, 1234–1242. doi:
10.1021/pr049882h
Craig, R., Cortens, J. P., and Beavis, R. C. (2005). The use of teotypic peptide libraries for pro-tein identification. Rapid Commun.
Mass Spectrom. 19, 1844–1850. doi:
10.1002/rcm.1992
Denison, F. C., Paul, A.-L., Zupanska, A. K., and Ferl, R. J. (2011). 14-3-3 proteins in plant physiology. Semin.
Cell Dev. Biol. 22, 720–727. doi:
10.1016/j.semcdb.2011.08.006 Dennison, W. C. (1990). “Chlorophyll
content,” in Seagrass Research Methods, eds R. C. Phillips and C. P.
McRoy (UNESCO), 83–85.
Diatchenko, L., Laut, Y. C., Campbellt, A. P., Chenchik, A., Moqadam, F., Huang, B., et al. (1996).
Suppression subtractive hybridiza-tion: a method for generating differentially regulated or tissue-specific cDNA probes. Proc. Natl.
Acad. Sci. U.S.A. 93, 6025–6030.
doi: 10.1073/pnas.93.12.6025
Mol. Ecol. 21, 1060–1080. doi:
10.1111/j.1365-294X.2011.05426.x Doney, S. C., Ruckelshaus, M., Emmett
Duffy, J., Barry, J. P., Chan, F., English, C. A., et al. (2002). Climate change impacts on marine ecosys-tems. Estuaries 25, 149–164. doi:
10.1007/BF02691304
Du, Z., Zhou, X., Li, L., and Su, Z. (2009). plantsUPS: a database of plants’ Ubiquitin Proteasome System. BMC Genomics 10:227. doi:
10.1186/1471-2164-10-227 Edge, S. E., Morgan, M. B., and Snell,
T. W. (2008). Temporal analy-sis of gene expression in a field population of the Scleractinian coral Montastraea faveolata. J. Exp.
Mar. Biol. Ecol. 355, 114–124. doi:
10.1016/j.jembe.2007.12.004 Elrad, D., Niyogi, K. K., and
Grossman, A. R. (2002). A major light-harvesting polypeptide of photosystem II functions in ther-mal dissipation. Plant Cell 14, 1801–1816. doi: 10.1105/tpc.002154 Escoubas, J. M., Lomas, M., LaRoche, J., and Falkowski, P. G. (1995).
Light intensity regulation of cab gene transcription is signaled by the redox state of the plasto-quinone pool. Proc. Natl. Acad.
Sci. U.S.A. 92, 10237–10241. doi:
10.1073/pnas.92.22.10237 Feder, M. E., and Walser, J.-C. (2005).
The biological limitations of tran-scriptomics in elucidating stress and stress responses. J. Evol. Biol.
18, 901–910. doi: 10.1111/j.1420-9101.2005.00921.x
Fenyö, D., Eriksson, J., and Beavis, R. (2010). “Mass spectrometric protein identification using the global proteome machine,” in Computational Biology, Methods in Molecular Biology, Vol. 673,
ed D. Fenyö (New York, NY: The Rockefeller University), 189–202.
doi: 10.1007/978-1-60761-842-3_11 Fernie, A. R., Carrari, F., and Sweetlove, L. J. (2004). Respiratory metabolism: glycolysis, the TCA cycle and mitochondrial elec-tron transport. Curr. Opin.
Plant Biol. 7, 254–261. doi:
10.1016/j.pbi.2004.03.007 Foret, S., Kassahn, K. S., Grasso, L.
C., Hayward, D. C., Iguchi, A., Ball, E. E., et al. (2007). Genomic and microarray approaches to coral reef conservation biology. Coral Reefs 26, 475–486. doi: 10.1007/s00338-007-0206-1
Fujita, Y. (1997). A study on the dynamic features of photosystem stoichiometry: accomplishments and problems for future studies.
Photosynth. Res. 53, 83–93. doi:
10.1023/A:1005870301868 Gagne, J. M., Smalle, J., Gingerich,
D. J., Walker, J. M., Yoo, S.-D., Yanagisawa, S., et al. (2004).
Arabidopsis EIN3-binding F-box 1 and 2 form ubiquitin-protein ligases that repress ethylene action and promote growth by directing EIN3 degradation. Proc. Natl. Acad.
Sci. U.S.A. 101, 6803–6808. doi:
10.1073/pnas.0401698101 Giordani, T., Natali, L., Maserti, B. E.,
Taddei, S., and Cavallini, A. (2000).
Characterization and expression of DNA sequences encoding puta-tive type-II metallothioneins in the seagrass Posidonia oceanica.
Plant Physiol. 123, 1571–1582. doi:
10.1104/pp.123.4.1571
Gracey, A. Y. (2007). Interpreting phys-iological responses to environmen-tal change through gene expres-sion profiling. J. Exp. Biol. 210, 1584–1592. doi: 10.1242/jeb.004333 Green, E. P., and Short, F. T. (2003).
World Atlas of Seagrasses. Prepared by the UNEP World Conservation Monitoring Centre. Berkeley, CA:
University of California Press.
Guo, Y., Xiao, P., Lei, S., Deng, F., Xiao, G. G., Liu, Y., et al. (2008). How is mRNA expression predictive for protein expression? A correlation study on human circulating mono-cytes. Acta Biochim. Biophys. Sin.
40, 426–436. doi:
Curr. Biol. 13, 2091–2096. doi:
10.1016/j.cub.2003.11.019 Hill, J. K., Griffiths, H. M., and
Thomas, C. D. (2010). “Climate change and evolutionary adapta-tions at species’ range margins,”
in Annual Review of Entomology, Vol. 56, eds M. R. Berenbaum, R. T. Carde, and G. E. Robinson, 143–159. doi: 10.1146/annurev-ento-120709-144746
Hofmann, G. E., Burnaford, J. L., and Fielman, K. T. (2005). Genomics-fueled approaches to current challenges in marine ecology.
Trends Ecol. Evol. 20, 305–311. doi:
10.1016/j.tree.2005.03.006 Huang, S.-S. C., Clarke, D. C., Gosline,
S. J. C., Labadorf, A., Chouinard, C. R., Gordon, W., et al. (2013).
Linking proteomic and transcrip-tional data through the interac-tome and epigenome reveals a map of oncogene-induced signal-ing. PLoS Comput. Biol. 9:e1002887.
doi: 10.1371/journal.pcbi.1002887 Huang, X. (1999). CAP3: a DNA
sequence assembly program.
Genome Res. 9, 868–877. doi:
10.1101/gr.9.9.868
Jiao, Y., Lau, O. S., and Deng, X. W.
(2007). Light-regulated transcrip-tional networks in higher plants.
Nat. Rev. Genet. 8, 217–230. doi:
10.1038/nrg2049
Jones, H., Ostrowski, M., and Scanlan, D. J. (2006). A suppression subtrac-tive hybridization approach reveals niche-specific genes that may be involved in predator avoidance in marine Synechococcus isolates.
Proc. Nat. Acad. Sci. U.S.A. 72, 2730–2737. doi: 10.1128/AEM.72.4.
2730-2737.2006
Karr, T. L. (2008). Application of pro-teomics to ecology and population biology. Heredity 100, 200–206. doi:
10.1038/sj.hdy.6801008
Kassahn, K. S., Crozier, R. H., Poertner, H. O., and Caley, M. J. (2009).
Animal performance and stress:
responses and tolerance limits at different levels of biological organisation. Biol. Rev. 84, 277–292.
doi: 10.1111/j.1469-185X.2008.
00073.x
Kendrick, M. D., and Chang, C. (2009).
Ethylene signaling: new levels of complexity and regulation. Curr.
Opin. Plant Biol. 11, 479–485. doi:
10.1016/j.pbi.2008.06.011 Larsen, P. F., Nielsen, E. E., Meier,
K., Olsvik, P. A., Hansen, M.
M., and Loeschcke, V. (2012).
Differences in salinity tolerance and gene expression between two populations of Atlantic cod (Gadus morhua) in response to salinity stress. Biochem. Genet. 50, 454–466. doi: 10.1007/s10528-011-9490-0
Lee, K.-S., Park, S. R., and Kim, Y. K.
(2007). Effects of irradiance, tem-perature, and nutrients on growth dynamics of seagrasses: a review.
www.frontiersin.org June 2013 | Volume 4 | Article 195|13
Dattolo et al. Posidonia oceanica acclimation at depth
J. Exp. Mar. Biol. Ecol. 350, 144–175.
doi: 10.1016/j.jembe.2007.06.016 Levitan, O., Kranz, S. A., Spungin, D.,
Prásil, O., Rost, B., and Berman-Frank, I. (2010). Combined effects of CO2 and light on the N2-fixing cyanobacterium Trichodesmium IMS101: a mechanistic view.
Plant Physiol. 154, 346–356. doi:
10.1104/pp.110.159285
Liu, L., Zhou, Y., Zhou, G., Ye, R., Zhao, L., Li, X., et al. (2008a).
Identification of early senescence-associated genes in rice flag leaves.
Plant Mol. Biol. 67, 37–55. doi:
10.1007/s11103-008-9300-1 Liu, X., Zhang, M., Duan, J., and
Wu, K. (2008b). Gene expression analysis of germinating rice seeds responding to high hydrostatic pressure. J. Plant Physiol. 165, 1855–1864. doi: 10.1016/j.jplph.
2008.05.004
Maathuis, F. J. M., Filatov, V., Herzyk, P.
C., Krijger, G. B., Axelsen, K., Chen, S., et al. (2003). Transcriptome anal-ysis of root transporters reveals par-ticipation of multiple gene fam-ilies in the response to cation stress. Plant J. 35, 675–692. doi:
10.1046/j.1365-313X.2003.01839.x Massa, S. I., Pearson, G. A., Aires, T.,
Kube, M., Olsen, J. L., Reinhardt, R., et al. (2011). Expressed sequence tags from heat-shocked seagrass Zostera noltii (Hornemann) from its southern distribution range.
Mar. Genomics 4, 181–188. doi:
10.1016/j.margen.2011.04.003 Matsumoto, T. K. (2006). Genes
uniquely expressed in vegetative and potassium chlorate induced floral buds of Dimocarpus lon-gan. Plant Sci. 170, 500–510. doi:
10.1016/j.plantsci.2005.09.016 Mazzuca, S., Spadafora, A., Filadoro,
D., Vannini, C., Marsoni, M., Cozza, R., et al. (2009). Seagrass light acclimation: 2-DE protein analy-sis in Posidonia leaves grown in chronic low light conditions. J. Exp.
Mar. Biol. Ecol. 374, 113–122. doi:
10.1016/j.jembe.2009.04.010 McArthur, L. C., and Boland, J. W.
(2006). The economic contri-bution of seagrass to secondary production in South Australia.
Ecol. Model. 196, 163–172. doi:
10.1016/j.ecolmodel.2006.02.030 Metzker, M. L. (2010). Sequencing
technologies – the next generation.
Nat. Rev. Genet. 11, 31–46. doi:
10.1038/nrg2626
Migliaccio, M., De Martino, F., Silvestre, F., and Procaccini, G.
(2005). Meadow-scale genetic structure in Posidonia oceanica.
Mar. Ecol. Prog. Ser. 304, 55–65. doi:
10.3354/meps304055
Moon, J., Parry, G., and Estelle, M.
(2004). The Ubiquitin-proteasome pathway and plant development.
Plant Cell 16, 3181–3195. doi:
10.1105/tpc.104.161220
Morozova, O., and Marra, M.
A. (2008). Applications of
Dennison, W. C., Duarte, C. M., Fourqurean, J. W., Heck, K. L. Jr., et al. (2006). A global crisis for seagrass ecosystems. Bioscience 56, 987–996. doi: 10.1641/0006-3568 (2006)56[987:AGCFSE]2.0.CO;2 Pascal, L. E., True, L. D., Campbell,
D. S., Deutsch, E. W., Risk, M., Coleman, I. M., et al. (2008).
Correlation of mRNA and protein levels: cell type-specific gene expres-sion of cluster designation anti-gens in the prostate. BMC Genomics 9:246. doi: 10.1186/1471-2164-9-246
Pasqualini, V., Pergent-martini, C., Clabaut, P., and Pergent, G. (1998).
Mapping of Posidonia oceanica using aerial photographs and side scan sonar: application off the island of Corsica (France). Estuar.
Coast. Shelf Sci. 47, 359–367. doi:
10.1006/ecss.1998.0361
Pirc, H. (1986). Seasonal aspects of photosynthesis in posidonia ocean-ica: influence of depth, tempera-ture aand ligth intensity. Aquat. Bot.
26, 203–212. doi: 10.1016/0304-3770(86)90021-5
Procaccini, G., Olsen, J. L., and Reusch, T. B. H. (2007). Contribution of genetics and genomics to seagrass biology and conservation. J. Exp.
Mar. Biol. Ecol. 350, 234–259. doi:
10.1016/j.jembe.2007.05.035 Pop, M., and Salzberg, S. L. (2008).
Bioinformatics challenges of new sequencing technology.
Trends Genet. 24, 142–149. doi:
10.1016/j.tig.2007.12.006 Portis, A. R. (2003). Rubisco
acti-vase – Rubisco’s catalytic chaper-one. Photosynth. Res. 75, 11–27. doi:
10.1023/A:1022458108678 Potuschak, T., Lechner, E., Parmentier,
Y., Yanagisawa, S., Grava, S., Koncz, C., et al. (2003). EIN3-dependent regulation of plant ethylene hor-mone signaling by two arabidopsis F box proteins: EBF1 and EBF2. Cell 115, 679–689. doi: 10.1016/S0092-8674(03)00968-1
Puthoff, D. P., and Smigocki, A. C.
(2007). Insect feeding-induced differential expression of Beta vulgaris root genes and their regulation by defense-associated
signals. Plant Cell Rep. 26, 71–84.
doi: 10.1007/s00299-006-0201-y Raab, S., Drechsel, G., Zarepour, M.,
Hartung, W., Koshiba, T., Bittner, F., et al. (2009). Identification of a novel E3 ubiquitin ligase that is required for suppres-sion of premature senescence in Arabidopsis. Plant J. 59, 39–51. doi:
10.1111/j.1365-313X.2009.03846.x Reusch, T. B. H., Veron, A. S., Preuss,
C., Weiner, J., Wissler, L., Beck, A., et al. (2008). Comparative analy-sis of expressed sequence tag (EST) libraries in the seagrass Zostera marina subjected to temperature stress. Mar. Biotechnol. (N.Y.) 10, 297–309. doi: 10.1007/s10126-007-9065-6
Richards, C. L., Rosas, U., Banta, J., Bhambhra, N., and Purugganan, M.
D. (2012). Genome-wide patterns of Arabidopsis gene expression in nature. PLoS Genet. 8, 482–495. doi:
10.1371/journal.pgen.1002662 Rogers, S., Girolami, M., Kolch, W.,
Waters, K. M., Liu, T., Thrall, B., et al. (2008). Investigating the correspondence between transcrip-tomic and proteomic expression profiles using coupled cluster mod-els. Bioinformatics 24, 2894–2900.
doi: 10.1093/bioinformatics/btn553 Ruggiero, M. V., Turk, R., and Procaccini, G. (2002). Genetic identity and homozygosity in North-Adriatic populations of Posidonia oceanica: an ancient, post-glacial clone? Conserv.
Genet. 3, 71–74. doi: 10.1023/
A:1014207122382
Schlacher-Hoenlinger, M. A., and Schlacher, T. A. (1998).
Accumulation, contamination, and seasonal variability of trace metals in the coastal zone – patterns in a seagrass meadow from the Mediterranean. Mar.
Biol. 131, 401–410. doi: 10.1007/
s002270050333
Schmidt, P. S., Serrao, E. A., Pearson, G. A., Riginos, C., Rawson, P.
D., Hilbish, T. J., et al. (2008).
Ecological genetics in the north Atlantic: environmental gradi-ents and adaptation at specific loci. Ecology 89, S91–S107. doi:
10.1890/07-1162.1
Serra, I. A., Nicastro, S., Mazzuca, S., Natali, L., Cavallini, A., and Innocenti, A. M. (2012a). Response to salt stress in seagrasses: PIP1;1 aquaporin antibody localization in Posidonia oceanica leaves. Aquat.
Bot. 104, 213–219. doi: 10.1016/j.
aquabot.2011.05.008
Serra, I. A., Lauritano, C., Dattolo, E., Puoti, A., Nicastro, S., Innocenti, A. M., et al. (2012b). Reference
genes assessment for the seagrass Posidonia oceanica in different salinity, pH and light conditions.
Mar. Biol. 159, 1269–1282. doi:
10.1007/s00227-012-1907-8 Sharon, Y., Levitan, O., Spungin,
D., Berman-Frank, I., and Beer, S. (2011). Photoacclimation of the seagrass Halophila stipu-lacea to the dim irradiance at its 48-meter depth limit. Limnol.
Oceanogr. 56, 357–362. doi:
10.4319/lo.2011.56.1.0357 Short, F. T., and Wyllie-Echeverria,
S. (1996). Natural and human-induced disturbance of seagrasses.
Environ. Conserv. 23, 17–27. doi:
10.1017/S0376892900038212 Spadafora, A., Filadoro, D., Mazzuca,
S., Bracale, M., Marsoni, M., Cardilio, M., et al. (2008). 2-DE polypeptide mapping of Posidonia oceanica leaves, a molecular tool for marine environment studies. Plant Biosyst. 142, 213–218. doi: 10.1080/
11263500802150316
Staden, R. (1996). The Staden sequence analysis package. Mol. Biotechnol. 5, 233–241. doi: 10.1007/BF02900361 Stapley, J., Reger, J., Feulner, P. G. D.,
Smadja, C., Galindo, J., Ekblom, R., et al. (2010). Adaptation genomics: the next generation.
Trends Ecol. Evol. 25, 705–712. doi:
10.1016/j.tree.2010.09.002 Thimm, O., Bläsing, O., Gibon, Y.,
Nagel, A., Meyer, S., Krüger, P., et al. (2004). MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological pro-cesses. Plant J. 37, 914–939. doi:
10.1111/j.1365-313X.2004.02016.x Thomas, C. D. (2010). Climate,
cli-mate change and range boundaries.
Diversity Distrib. 16, 488–495. doi:
10.1111/j.1472-4642.2010.00642.x Thomas, C. D., Cameron, A., Green,
R. E., Bakkenes, M., Beaumont, L. J., Collingham, Y. C., et al.
(2004). Extinction risk from climate change. Nature 427, 145–148. doi:
10.1038/nature02121
Touchette, B., and Burkholder, J. (2000). Overview of the physiological ecology of carbon metabolism in seagrasses. J. Exp.
Mar. Biol. Ecol. 250, 169–205. doi:
10.1016/S0022-0981(00)00196-9 Vogel, C., and Marcotte, E. M. (2012).
Insights into the regulation of pro-tein abundance from proteomic and transcriptomic analyses. Nat. Rev.
Genet. 13, 227–232. doi: 10.1038/
nrg3185
Warnau, M., Fowler, S. W., and Teyssié, J. L. (1996). Biokinetics of selected heavy metals and radionuclides in two marine macrophytes: the
Frontiers in Plant Science | Plant Proteomics June 2013 | Volume 4 | Article 195|14
Dattolo et al. Posidonia oceanica acclimation at depth
seagrass Posidonia oceanica and the alga Caulerpa taxifolia. Mar.
Environ. Res. 41, 343–362. doi:
10.1016/0141-1136(95)00025-9 Waycott, M., Duarte, C. M., Carruthers,
T. J. B., Orth, R. J., Dennison, W.
C., Olyarnik, S., et al. (2009).
Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc. Natl. Acad. Sci.
U.S.A. 106, 12377–12381. doi:
10.1073/pnas.0905620106 Winters, G., Nelle, P., Fricke, B., Rauch,
G., and Reusch, T. B. H. (2011).
Effects of a simulated heat wave on photophysiology and gene expres-sion of high- and low-latitude pop-ulations of Zostera marina. Mar.
Ecol. Prog. Ser. 435, 83–95. doi:
10.3354/meps09213
Wissler, L., Dattolo, E., Moore, A.
D., Reusch, T. B. H., Olsen, J. L., Migliaccio, M., et al. (2009).
Dr. Zompo: an online data
repository for Zostera marina and Posidonia oceanica ESTs.
Database (Oxford) 2009:bap009.
doi: 10.1093/database/bap009 Yamazaki, J.-Y., Suzuki, T., Maruta, E.,
and Kamimura, Y. (2005). The sto-ichiometry and antenna size of the two photosystems in marine green algae, Bryopsis maxima and Ulva pertusa, in relation to the light envi-ronment of their natural habitat.
J. Exp. Bot. 56, 1517–1523. doi:
10.1093/jxb/eri147
Yamori, W., Masumoto, C., Fukayama, H., and Makino, A. (2012). Rubisco activase is a key regulator of non-steady-state photosynthesis at any leaf temperature and, to a lesser extent, of steady-state photosynthe-sis at high temperature. Plant J.
71, 871–880. doi: 10.1111/j.1365-313X.2012.05041.x
Yin, Z., Meng, F., Song, H., Wang, X., Xu, X., and Yu, D. (2010).
Expression quantitative trait loci analysis of two genes encoding rubisco activase in soybean. Plant Physiol. 152, 1625–1637. doi:
10.1104/pp.109.148312
Zouari, N., Ben Saad, R., Legavre, T., Azaza, J., Sabau, X., Jaoua, M., et al. (2007). Identification and sequencing of ESTs from the halophyte grass Aeluropus littoralis. Gene 404, 61–69. doi:
10.1016/j.gene.2007.08.021 Conflict of Interest Statement: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Received: 16 February 2013; accepted:
27 May 2013; published online: 17 June 2013.
Citation: Dattolo E, Gu J, Bayer PE, Mazzuca S, Serra IA, Spadafora A, Bernardo L, Natali L, Cavallini A and Procaccini G (2013) Acclimation to different depths by the marine angiosperm Posidonia oceanica: tran-scriptomic and proteomic profiles. Front.
Plant Sci. 4:195. doi: 10.3389/fpls.
2013.00195
This article was submitted to Frontiers in Plant Proteomics, a specialty of Frontiers in Plant Science.
Copyright © 2013 Dattolo, Gu, Bayer, Mazzuca, Serra, Spadafora, Bernardo, Natali, Cavallini and Procaccini.
This is an open-access article dis-tributed under the terms of the Creative Commons Attribution License, which permits use, distribution and repro-duction in other forums, provided the original authors and source are credited and subject to any copyright notices concerning any third-party graphics etc.
www.frontiersin.org June 2013 | Volume 4 | Article 195|15